He Zhang

Animal behavior is linked to the gene regulatory network (GRN) coordinating gene expression in the brain. Eusocial honeybees, with their natural behavioral plasticity, provide an excellent model for exploring the connection between brain activity and behavior. Using single-nucleus RNA sequencing and spatial transcriptomics, we analyze the expression patterns of brain cells associated with the behavioral maturation from nursing to foraging. Integrating spatial and cellular data uncovered cell-type and spatial heterogeneity in GRN organization. Interestingly, the stripe regulon is explicitly activated in foragers’ small Keyon cells, which are implicated in spatial learning and navigation. When worker age is controlled in artificial colonies, stripe and its key targets remained highly expressed in the KC regions of bees performing foraging tasks. These findings suggest that specific GRNs coordinate individual brain cell activity during behavioral transitions, shedding light on GRN-driven brain heterogeneity and its role in the division of labor of social life.

Animal behavior is associated with the gene regulatory network (GRN) coordinating gene expression levels in the brain. The eusocial honeybees with natural behavioral plasticity provide an ideal model for studying the relationship between brain activity and behaviors. Here, using single-nucleus RNA sequencing and spatial transcriptomics, we profile the expression changes of 121,247 brain cells associated with the behavioral maturation of honeybees from nursing to foraging outside. We identified 24 subpopulations of brain cells, including Kenyon, glia, optic lobes, and olfactory projection neurons. Compared to non-social insects, Drosophila, the Keyon cells display a high diversity in the mushroom body of honeybees. Integrating spatial and cellular profiles finds that the mushroom body and optic lobes show specifically high activities of the regulons led by different transcription factors. The stripe regulon is activated explicitly in the foragers’ small- and middle-type Keyon cells implicated in spatial learning and navigation behavior. These suggest that the activity of individual brain cells is coordinated by specific GRNs during the behavioral transition of honeybees. Our results provide a deeper understanding of the behavior-associated brain heterogeneity in GRN, which may be a key driver for the division of labor in social life.

The past two decades has witnessed a remarkable increase in the number of microbial genomes retrieved from marine systems^1,2. However, it has remained challenging to translate this marine genomic diversity into biotechnological and biomedical applications^3,4. Here we recovered 43,191 bacterial and archaeal genomes from publicly available marine metagenomes, encompassing a wide range of diversity with 138 distinct phyla, redefining the upper limit of marine bacterial genome size and revealing complex trade-offs between the occurrence of CRISPR–Cas systems and antibiotic resistance genes. In silico bioprospecting of these marine genomes led to the discovery of a novel CRISPR–Cas9 system, ten antimicrobial peptides, and three enzymes that degrade polyethylene terephthalate. In vitro experiments confirmed their effectiveness and efficacy. This work provides evidence that global-scale sequencing initiatives advance our understanding of how microbial diversity has evolved in the oceans and is maintained, and demonstrates how such initiatives can be sustainably exploited to advance biotechnology and biomedicine.

Teleosts, the most species-rich group of jawed vertebrates, have evolved a remarkable diversity of primitive and specialized features that provide a valuable resource for understanding vertebrate evolution. Here, we collected a comprehensive genome dataset of fish, including 115 newly sequenced species, to fill genome gaps for seven orders. By combining the phylogenetic and fossil records of teleosts, we observed that they were relatively scarce from the early to middle Triassic but quickly flourished following the massive extinction event at the end of the Triassic. This rapid radiation coincided with global temperature increases and the fragmentation of Gondwana, implying a positive correlation between temperature rise, tectonic plate movements, and teleost radiations. Our data also revealed that the end-Triassic extinction event had a greater impact on teleost radiation than the Permian-Triassic extinction. We identified a core set of regulatory elements related to aquatic adaptation traits such as swim bladder functional shift and structural specialization of pectoral fin, which were crucial for the adaptation of teleosts to their broad ecological niches. Functional experiments validated the regulatory roles of these conserved elements on the formation of specialized homologous organs in teleosts. Overall, our findings shed light on the links between teleost speciation bursts with geological events, and genetic innovations that have shaped extant teleost biodiversity.

Changes in developmental gene regulatory networks (dGRNs) underlie much of the diversity of life, but the evolutionary mechanisms that operate on regulatory interactions remain poorly understood. Closely related species with extreme phenotypic divergence provide a valuable window into the genetic and molecular basis for changes in dGRNs and their relationship to adaptive changes in organismal traits. Here we analyse genomes, epigenomes and transcriptomes during early development in two Heliocidaris sea urchin species that exhibit highly divergent life histories and in an outgroup species. Positive selection and chromatin accessibility modifications within putative regulatory elements are enriched on the branch leading to the derived life history, particularly near dGRN genes. Single-cell transcriptomes reveal a dramatic delay in cell fate specification in the derived state, which also has far fewer open chromatin regions, especially near conserved cell fate specification genes. Experimentally perturbing key transcription factors reveals profound evolutionary changes to early embryonic patterning events, disrupting regulatory interactions previously conserved for ~225 million years. These results demonstrate that natural selection can rapidly reshape developmental gene expression on a broad scale when selective regimes abruptly change. More broadly, even highly conserved dGRNs and patterning mechanisms in the early embryo remain evolvable under appropriate ecological circumstances.

The Bicolor Angelfish, Centropyge bicolor, is a tropical coral reef fish. It is named for its striking two-color body. However, a lack of high-quality genomic data means little is known about the genome of this species. Here, we present a chromosome-level C. bicolor genome constructed using Hi-C data. The assembled genome is 650 Mbp in size, with a scaffold N50 value of 4.4 Mbp, and a contig N50 value of 114 Kbp. Protein-coding genes numbering 21,774 were annotated. Our analysis will help others to choose the most appropriate de novo genome sequencing strategy based on resources and target applications. To the best of our knowledge, this is the first chromosome-level genome for the Pomacanthidae family, which might contribute to further studies exploring coral reef fish evolution, diversity and conservation.

The Bicolor Angelfish, Centropyge bicolor , is a tropical coral reef fish. It is named for its striking two-color body. However, a lack of high-quality genomic data means little is known about the genome of this species. Here, we present a chromosome-level C. bicolor genome constructed using Hi-C data. The assembled genome is 650 Mbp in size, with a scaffold N50 value of 4.4 Mbp, and a contig N50 value of 114 Kbp. Protein-coding genes numbering 21,774 were annotated. Our analysis will help others to choose the most appropriate de novo genome sequencing strategy based on resources and target applications. To the best of our knowledge, this is the first chromosome-level genome for the Pomacanthidae family, which might contribute to further studies exploring coral reef fish evolution, diversity and conservation.

The humpback puffer, Tetraodon palembangensis, is a poisonous freshwater pufferfish species mainly distributed in Southeast Asia (Thailand, Laos, Malaysia and Indonesia). The humpback puffer has many interesting biological features, such as inactivity, tetrodotoxin production and body expansion. Here, we report the first chromosome-level genome assembly of the humpback puffer. The genome size is 362 Mb, with a contig N50 value of ∼1.78 Mb and a scaffold N50 value of ∼15.8 Mb. Based on this genome assembly, ∼61.5 Mb (18.11%) repeat sequences were identified, 19,925 genes were annotated, and the function of 90.01% of these genes could be predicted. Finally, a phylogenetic tree of ten teleost fish species was constructed. This analysis suggests that the humpback puffer and T. nigroviridis share a common ancestor 18.1 million years ago (MYA), and diverged from T. rubripes 45.8 MYA. The humpback puffer genome will be a valuable genomic resource to illustrate possible mechanisms of tetrodotoxin synthesis and tolerance.